Sperm DNA fragmentation in cryopreserved samples from subjects with different cancers
Lara Tamburrino A , Marta Cambi A , Sara Marchiani A , Ilaria Manigrasso A , Selene Degl’Innocenti B , Gianni Forti A , Mario Maggi A , Elisabetta Baldi A C and Monica Muratori A C
+ Author Affiliations
- Author Affiliations
A Department of Biomedical, Experimental and Clinical Sciences, Centre of Excellence DeNothe, University of Florence, Viale Pieraccini 6, I-50139 Florence, Italy.
B Azienda Ospedaliera-Universitaria Careggi, Florence, Viale Pieraccini 6, I-50139 Florence, Italy.
C Corresponding authors. Emails: elisabetta.baldi@unifi.it; monica.muratori@unifi.it
Reproduction, Fertility and Development 29(4) 637-645 https://doi.org/10.1071/RD15190
Submitted: 18 March 2015 Accepted: 14 September 2015 Published: 14 October 2015
Abstract
Sperm cryopreservation is widely used by cancer patients undergoing chemo- or radiotherapy. Evidence suggests that IVF outcome with cryopreserved spermatozoa from cancer patients is less successful. To determine whether sperm DNA fragmentation (SDF) is involved in the lower fertilising ability of cryopreserved spermatozoa of cancer patients, SDF was evaluated in thawed spermatozoa from 78 men affected by different cancers and 53 men with non-cancer pathologies. SDF was assessed by the terminal deoxyribonucleotidyl transferase-mediated dUTP–digoxigenin nick end-labelling (TUNEL), propidium iodide (PI), flow cytometry procedure, which allows determination of two different cell populations (PIbrighter and PIdimmer) and thus to determine the percentage of DNA fragmented sperm in both. PIdimmer spermatozoa are totally unviable, whereas PIbrighter spermatozoa with SDF may be motile and morphologically normal, having higher biological relevance in the reproductive process. We found that the proportion of DNA fragmented PIbrighter cells was significantly higher in thawed spermatozoa from cancer than non-cancer patients. Moreover, a positive correlation was found between the degree of DNA fragmentation and sperm motility in the PIbrighter population of spermatozoa from cancer patients that wasn’t seen in non-cancer patients. The results of the present study suggest that higher SDF levels may contribute to the lower IVF success of cryopreserved spermatozoa from cancer patients and that evaluation of SDF could complement genetic counselling as part of the routine management of cancer patients who seek fertility preservation.
Additional keywords: cancer patients, flow cytometry, propidium iodide, terminal deoxyribonucleotidyl transferase-mediated dUTP–digoxigenin nick end-labelling (TUNEL).
References
Agarwal, A., and Allamaneni, S. S. (2005). Disruption of spermatogenesis by the cancer disease process. J. Natl Cancer Inst. Monogr. 2005, 9–12.| Disruption of spermatogenesis by the cancer disease process.Crossref | GoogleScholarGoogle Scholar |
Agarwal, A., Ranganathan, P., Kattal, N., Pasqualotto, F., Hallak, J., Khayal, S., and Mascha, E. (2004). Fertility after cancer: a prospective review of assisted reproductive outcome with banked semen specimens. Fertil. Steril. 81, 342–348.
| Fertility after cancer: a prospective review of assisted reproductive outcome with banked semen specimens.Crossref | GoogleScholarGoogle Scholar | 14967371PubMed |
Ahmadi, A., and Ng, S. C. (1999). Fertilizing ability of DNA-damaged spermatozoa. J. Exp. Zool. 284, 696–704.
| Fertilizing ability of DNA-damaged spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2Fgt1OgsA%3D%3D&md5=d2db7b3d25c2141b580fd19fec26a8e8CAS | 10531556PubMed |
Bizet, P., Saias-Magnan, J., Jouve, E., Grillo, J. M., Karsenty, G., Metzler-Guillemain, C., and Perrin, J. (2012). Sperm cryopreservation before cancer treatment: a 15-year monocentric experience. Reprod. Biomed. Online 24, 321–330.
| Sperm cryopreservation before cancer treatment: a 15-year monocentric experience.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC383otFOjsA%3D%3D&md5=54ae22a3d4ce772d1974579252b7a16eCAS | 22285245PubMed |
Botchan, A., Karpol, S., Lehavi, O., Paz, G., Kleiman, S. E., Yogev, L., Yavetz, H., and Hauser, R. (2013). Preservation of sperm of cancer patients: extent of use and pregnancy outcome in a tertiary infertility center. Asian J. Androl. 15, 382–386.
| Preservation of sperm of cancer patients: extent of use and pregnancy outcome in a tertiary infertility center.Crossref | GoogleScholarGoogle Scholar | 23524529PubMed |
Bujan, L., Walschaerts, M., Brugnon, F., Daudin, M., Berthaut, I., Auger, J., Saias, J., Szerman, E., Moinard, N., Rives, N., and Hennebicq, S. (2014). Impact of lymphoma treatments on spermatogenesis and sperm deoxyribonucleic acid: a multicenter prospective study from the CECOS network. Fertil. Steril. 102, 667–674.e3.
| Impact of lymphoma treatments on spermatogenesis and sperm deoxyribonucleic acid: a multicenter prospective study from the CECOS network.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFyhtLzM&md5=f4d33f67fa79296eb1dd4f54bf614eefCAS | 25044088PubMed |
Chung, K., Irani, J., Knee, G., Efymow, B., Blasco, L., and Patrizio, P. (2004). Sperm cryopreservation for male patients with cancer: an epidemiological analysis at the University of Pennsylvania. Eur. J. Obstet. Gynecol. Reprod. Biol. 113, S7–S11.
| Sperm cryopreservation for male patients with cancer: an epidemiological analysis at the University of Pennsylvania.Crossref | GoogleScholarGoogle Scholar | 15041122PubMed |
Clarke, G. N., Bourne, H., Hill, P., Johnston, W. I., Speirs, A., McBain, J. C., and Baker, H. W. (1997). Artificial insemination and in-vitro fertilization using donor spermatozoa: a report on 15 years of experience. Hum. Reprod. 12, 722–726.
| Artificial insemination and in-vitro fertilization using donor spermatozoa: a report on 15 years of experience.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2szgtlSjsw%3D%3D&md5=2988feb852b5cb5e30430bc5e77b7561CAS | 9159432PubMed |
Degl’Innocenti, S., Filimberti, E., Magini, A., Krausz, C., Lombardi, G., Fino, M. G., Rastrelli, G., Maggi, M., and Baldi, E. (2013). Semen cryopreservation for men banking for oligospermia, cancers, and other pathologies: prediction of post-thaw outcome using basal semen quality. Fertil. Steril. 100, 1555–1563.e3.
| Semen cryopreservation for men banking for oligospermia, cancers, and other pathologies: prediction of post-thaw outcome using basal semen quality.Crossref | GoogleScholarGoogle Scholar | 24034937PubMed |
Derijck, A., van der Heijden, G., Giele, M., Philippens, M., and de Boer, P. (2008). DNA double-strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation. Hum. Mol. Genet. 17, 1922–1937.
| DNA double-strand break repair in parental chromatin of mouse zygotes, the first cell cycle as an origin of de novo mutation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXntFOkt7Y%3D&md5=6c5ddfba3d27bdb77b76d3b3346b09cbCAS | 18353795PubMed |
Domínguez-Fandos, D., Camejo, M. I., Ballescà, J. L., and Oliva, R. (2007). Human sperm DNA fragmentation: correlation of TUNEL results as assessed by flow cytometry and optical microscopy. Cytometry A 71A, 1011–1018.
| Human sperm DNA fragmentation: correlation of TUNEL results as assessed by flow cytometry and optical microscopy.Crossref | GoogleScholarGoogle Scholar |
Edelstein, A., Yavetz, H., Kleiman, S. E., Botchan, A., Hauser, R., Paz, G., and Yogev, L. (2008). Deoxyribonucleic acid-damaged sperm in cryopreserved–thawed specimens from cancer patients and healthy men. Fertil. Steril. 90, 205–208.
| Deoxyribonucleic acid-damaged sperm in cryopreserved–thawed specimens from cancer patients and healthy men.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpslKls7w%3D&md5=9e73847e297a529b591cc6189f51bef7CAS | 17658528PubMed |
Fatehi, A. N., Bevers, M. M., Schoevers, E., Roelen, B. A., Colenbrander, B., and Gadella, B. M. (2006). DNA damage in bovine sperm does not block fertilization and early embryonic development but induces apoptosis after the first cleavages. J. Androl. 27, 176–188.
| DNA damage in bovine sperm does not block fertilization and early embryonic development but induces apoptosis after the first cleavages.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit12jtb0%3D&md5=9e406ca43839a4727456ab3c383681bbCAS | 16304212PubMed |
Gandini, L., Lombardo, F., Lenzi, A., Spanò, M., and Dondero, F. (2006). Cryopreservation and sperm DNA integrity. Cell Tissue Bank. 7, 91–98.
| Cryopreservation and sperm DNA integrity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltVOitLo%3D&md5=b2f415562f8ad35e8dcc8085d4531dd3CAS | 16732411PubMed |
Hallak, J., Kolletis, P. N., and Sekhon, V. S. (1999). Sperm cryopreservation in patients with testicular cancer. Urology 54, 894–899.
| Sperm cryopreservation in patients with testicular cancer.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FivFCrtg%3D%3D&md5=5c2f73ac793b3f95a4382d1243123d21CAS | 10565754PubMed |
Henkel, R., Hoogendijk, C. F., Bouic, P. J., and Kruger, T. F. (2010). TUNEL assay and SCSA determine different aspects of sperm DNA damage. Andrologia 42, 305–313.
| TUNEL assay and SCSA determine different aspects of sperm DNA damage.Crossref | GoogleScholarGoogle Scholar | 20860629PubMed |
Herrero, M. B., Delbes, G., Chung, J. T., Son, W. Y., Holzer, H., Buckett, W., and Chan, P. (2013). Case report: the use of annexin V coupled with magnetic activated cell sorting in cryopreserved spermatozoa from a male cancer survivor: healthy twin newborns after two previous ICSI failures. J. Assist. Reprod. Genet. 30, 1415–1419.
| Case report: the use of annexin V coupled with magnetic activated cell sorting in cryopreserved spermatozoa from a male cancer survivor: healthy twin newborns after two previous ICSI failures.Crossref | GoogleScholarGoogle Scholar | 24057155PubMed |
Kelleher, S., Wishart, S. M., Liu, P. Y., Turner, L., Di Pierro, I., Conway, A. J., and Handelsman, D. J. (2001). Long-term outcomes of elective human sperm cryostorage. Hum. Reprod. 16, 2632–2639.
| Long-term outcomes of elective human sperm cryostorage.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3MnotVCktw%3D%3D&md5=8c9499ecb442e18b813590460def795cCAS | 11726587PubMed |
Lass, A., Akagbosu, F., and Brinsden, P. (2001). Sperm banking and assisted reproduction treatment for couples following cancer treatment of the male partner. Hum. Reprod. Update 7, 370–377.
| Sperm banking and assisted reproduction treatment for couples following cancer treatment of the male partner.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD38%2Fis1Gitg%3D%3D&md5=6cab969a77b90ffb0024a9ed58d16929CAS | 11476349PubMed |
Marchiani, S., Tamburrino, L., Maoggi, A., Vannelli, G. B., Forti, G., Baldi, E., and Muratori, M. (2007). Characterization of M540 bodies in human semen: evidence that they are apoptotic bodies. Mol. Hum. Reprod. 13, 621–631.
| Characterization of M540 bodies in human semen: evidence that they are apoptotic bodies.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVSgtL7E&md5=8eaf9dd7f073344f0af4410ce2187ae9CAS | 17584827PubMed |
Marchiani, S., Tamburrino, L., Giuliano, L., Nosi, D., Sarli, V., Gandini, L., Piomboni, P., Belmonte, G., Forti, G., Baldi, E., and Muratori, M. (2011). Sumo1-ylation of human spermatozoa and its relationship with semen quality. Int. J. Androl. 34, 581–593.
| Sumo1-ylation of human spermatozoa and its relationship with semen quality.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XivFOgt78%3D&md5=3b36c0173095a03c361304772ef54956CAS | 21039605PubMed |
Marchiani, S., Tamburrino, L., Olivito, B., Betti, L., Azzari, C., Forti, G., Baldi, E., and Muratori, M. (2014a). Characterization and sorting of flow cytometric populations in human semen. Andrology 2, 394–401.
| Characterization and sorting of flow cytometric populations in human semen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmvF2ks7Y%3D&md5=7192cfe4011e3e6add0b09b1a2a43a2eCAS | 24700807PubMed |
Marchiani, S., Tamburrino, L., Ricci, B., Nosi, D., Cambi, M., Piomboni, P., Belmonte, G., Forti, G., Muratori, M., and Baldi, E. (2014b). SUMO1 in human sperm: new targets, role in motility and morphology and relationship with DNA damage. Reproduction 148, 453–467.
| SUMO1 in human sperm: new targets, role in motility and morphology and relationship with DNA damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvFyhtr7O&md5=60d86a0403097f998620d5b5fcc833e8CAS | 25118297PubMed |
McDowell, S., Harrison, K., Kroon, B., Ford, E., and Yazdani, A. (2013). Sperm DNA fragmentation in men with malignancy. Fertil. Steril. 99, 1862–1866.
| Sperm DNA fragmentation in men with malignancy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjsFyjsrg%3D&md5=f7138d0c2abdd580543b6fd1ed11ecffCAS | 23481280PubMed |
Ménézo, Y., Dale, B., and Cohen, M. (2010). DNA damage and repair in human oocytes and embryos: a review. Zygote 18, 357–365.
| DNA damage and repair in human oocytes and embryos: a review.Crossref | GoogleScholarGoogle Scholar | 20663262PubMed |
Meseguer, M., Santiso, R., Garrido, N., and Fernandez, J. L. (2008). The effect of cancer on sperm DNA fragmentation as measured by the sperm chromatin dispersion test. Fertil. Steril. 90, 225–227.
| The effect of cancer on sperm DNA fragmentation as measured by the sperm chromatin dispersion test.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpslKls7s%3D&md5=4ea971226e618cd2c4052df49c51d01fCAS | 17959174PubMed |
Moskovtsev, S. I., Willis, J., and Mullen, J. B. (2006). Age-related decline in sperm deoxyribonucleic acid integrity in patients evaluated for male infertility. Fertil. Steril. 85, 496–499.
| Age-related decline in sperm deoxyribonucleic acid integrity in patients evaluated for male infertility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xit12itro%3D&md5=49186cbd1312655968e17abfc8d174c9CAS | 16595239PubMed |
Muratori, M., Forti, G., and Baldi, E. (2008a). Comparing flow cytometry and fluorescence microscopy for analyzing human sperm DNA fragmentation by TUNEL labeling. Cytometry A 73A, 785–787.
| Comparing flow cytometry and fluorescence microscopy for analyzing human sperm DNA fragmentation by TUNEL labeling.Crossref | GoogleScholarGoogle Scholar |
Muratori, M., Marchiani, S., Tamburrino, L., Tocci, V., Failli, P., Forti, G., and Baldi, E. (2008b). Nuclear staining identifies two populations of human sperm with different DNA fragmentation extent and relationship with semen parameters. Hum. Reprod. 23, 1035–1043.
| Nuclear staining identifies two populations of human sperm with different DNA fragmentation extent and relationship with semen parameters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1agsr8%3D&md5=d1cb0076ce6c12143d5feb814c7405beCAS | 18326515PubMed |
Muratori, M., Tamburrino, L., Tocci, V., Costantino, A., Marchiani, S., Giachini, C., Laface, I., Krausz, C., Meriggiola, M. C., Forti, G., and Baldi, E. (2010). Small variations in crucial steps of TUNEL assay coupled to flow cytometry greatly affect measures of sperm DNA fragmentation. J. Androl. 31, 336–345.
| Small variations in crucial steps of TUNEL assay coupled to flow cytometry greatly affect measures of sperm DNA fragmentation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1KmsbvI&md5=57eff135cad2507712955995c117a2d3CAS | 19959824PubMed |
Muratori, M., Tamburrino, L., Marchiani, S., Cambi, M., Olivito, B., Azzari, C., Forti, G., and Baldi, E. (2015). Investigation on the origin of sperm DNA fragmentation: role of apoptosis, immaturity and oxidative stress. Mol. Med. 21, 109–122.
| Investigation on the origin of sperm DNA fragmentation: role of apoptosis, immaturity and oxidative stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXpvFKhsbc%3D&md5=056263b2c92db0964eee4c8cc2f1426aCAS | 25786204PubMed |
Nordqvist, S., Sydsjö, G., Lampic, C., Åkerud, H., Elenis, E., and Skoog Svanberg, A. (2014). Sexual orientation of women does not affect outcome of fertility treatment with donated sperm. Hum. Reprod. 29, 704–711.
| Sexual orientation of women does not affect outcome of fertility treatment with donated sperm.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2czmt1ektw%3D%3D&md5=74a16893a916e23dfb564c46b5491cc3CAS | 24435777PubMed |
O’Flaherty, C., Vaisheva, F., Hales, B. F., Chan, P., and Robaire, B. (2008). Characterization of sperm chromatin quality in testicular cancer and Hodgkin’s lymphoma patients prior to chemotherapy. Hum. Reprod. 23, 1044–1052.
| Characterization of sperm chromatin quality in testicular cancer and Hodgkin’s lymphoma patients prior to chemotherapy.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXlt1ags7k%3D&md5=5ac7839028360eaa870f3d48257b144cCAS | 18346994PubMed |
Pérez-Cerezales, S., Martínez-Páramo, S., Beirão, J., and Herráez, M. P. (2010). Fertilization capacity with rainbow trout DNA-damaged sperm and embryo developmental success. Reproduction 139, 989–997.
| Fertilization capacity with rainbow trout DNA-damaged sperm and embryo developmental success.Crossref | GoogleScholarGoogle Scholar | 20357047PubMed |
Ping, P., Gu, B. H., Li, P., Huang, Y. R., and Li, Z. (2014). Fertility outcome of patients with testicular tumor: before and after treatment. Asian J. Androl. 16, 107–111.
| Fertility outcome of patients with testicular tumor: before and after treatment.Crossref | GoogleScholarGoogle Scholar | 24369141PubMed |
Ragni, G., Somigliana, E., Restelli, L., Salvi, R., Arnoldi, M., and Paffoni, A. (2003). Sperm banking and rate of assisted reproduction treatment: insights from a 15-year cryopreservation program for male cancer patients. Cancer 97, 1624–1629.
| Sperm banking and rate of assisted reproduction treatment: insights from a 15-year cryopreservation program for male cancer patients.Crossref | GoogleScholarGoogle Scholar | 12655518PubMed |
Ribas-Maynou, J., Fernández-Encinas, A., García-Peiró, A., Prada, E., Abad, C., Amengual, M. J., Navarro, J., and Benet, J. (2014). Human semen cryopreservation: a sperm DNA fragmentation study with alkaline and neutral Comet assay. Andrology 2, 83–87.
| Human semen cryopreservation: a sperm DNA fragmentation study with alkaline and neutral Comet assay.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXitVSqtL7O&md5=4f4c9abb5af6308b83cddc062afd751fCAS | 24255006PubMed |
Ribeiro, T. M., Bertolla, R. P., Spaine, D. M., Fraietta, R., Ortiz, V., and Cedenho, A. P. (2008). Sperm nuclear apoptotic DNA fragmentation in men with testicular cancer. Fertil. Steril. 90, 1782–1786.
| Sperm nuclear apoptotic DNA fragmentation in men with testicular cancer.Crossref | GoogleScholarGoogle Scholar | 18068165PubMed |
Robinson, L., Gallos, I. D., Conner, S. J., Rajkhowa, M., Miller, D., Lewis, S., Kirkman-Brown, J., and Coomarasamy, A. (2012). The effect of sperm DNA fragmentation on miscarriage rates: a systematic review and meta-analysis. Hum. Reprod. 27, 2908–2917.
| The effect of sperm DNA fragmentation on miscarriage rates: a systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtlymsbbI&md5=7b92ad05f557e8c6ed3727b3c5f6bbc3CAS | 22791753PubMed |
Rofeim, O., and Gilbert, B. R. (2004). Normal semen parameters in cancer patients presenting or cryopreservation before gonadotoxic therapy. Fertil. Steril. 82, 505–506.
| Normal semen parameters in cancer patients presenting or cryopreservation before gonadotoxic therapy.Crossref | GoogleScholarGoogle Scholar | 15302317PubMed |
Said, T. M., Tellez, S., Evenson, D. P., and Del Valle, A. P. (2009). Assessment of sperm quality, DNA integrity and cryopreservation protocols in men diagnosed with testicular and systemic malignancies. Andrologia 41, 377–382.
| Assessment of sperm quality, DNA integrity and cryopreservation protocols in men diagnosed with testicular and systemic malignancies.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1MjktFOqug%3D%3D&md5=572ea6c4154c4f19a46c962b519bdc65CAS | 19891636PubMed |
Schmid, T. E., Eskenazi, B., Baumgartner, A., Marchetti, F., Young, S., Weldon, R., Anderson, D., and Wyrobek, A. J. (2007). The effects of male age on sperm DNA damage in healthy non-smokers. Hum. Reprod. 22, 180–187.
| The effects of male age on sperm DNA damage in healthy non-smokers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlChtbzE&md5=32d9789d72b3e898a6cc0aab293c61b3CAS | 17053003PubMed |
Smit, M., van Casteren, N. J., Wildhagen, M. F., Romijn, J. C., and Dohle, G. R. (2010). Sperm DNA integrity in cancer patients before and after cytotoxic treatment. Hum. Reprod. 25, 1877–1883.
| Sperm DNA integrity in cancer patients before and after cytotoxic treatment.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXptlaltb4%3D&md5=a2301b26655f24f3e5f661fc5abf6c51CAS | 20551071PubMed |
Ståhl, O., Eberhard, J., Cavallin-Ståhl, E., Jepson, K., Friberg, B., Tingsmark, C., Spanò, M., and Giwercman, A. (2009). Sperm DNA integrity in cancer patients: the effect of disease and treatment. Int. J. Androl. 32, 695–703.
| Sperm DNA integrity in cancer patients: the effect of disease and treatment.Crossref | GoogleScholarGoogle Scholar | 19178596PubMed |
Tamburrino, L., Marchiani, S., Montoya, M., Marino, F. E., Natali, I., Cambi, M., Forti, G., Baldi, E., and Muratori, M. (2012). Mechanisms and clinical correlates of sperm DNA damage. Asian J. Androl. 14, 24–31.
| Mechanisms and clinical correlates of sperm DNA damage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjs1ajtQ%3D%3D&md5=9ef7b2e56858b0a243a21b3ae5704647CAS | 22138903PubMed |
Tomlinson, M. J., Pooley, K., Pierce, A., and Hopkisson, J. F. (2010). Sperm donor recruitment within an NHS fertility service since the removal of anonymity. Hum. Fertil. (Camb.) 13, 159–167.
| Sperm donor recruitment within an NHS fertility service since the removal of anonymity.Crossref | GoogleScholarGoogle Scholar | 20849201PubMed |
van Casteren, N. J., van Santbrink, E. J. P., van Inzen, W., Romijn, J. C., and Dohle, G. R. (2008). Use rate and assisted reproduction technologies outcome of cryopreserved semen from 629 cancer patients. Fertil. Steril. 90, 2245–2250.
| Use rate and assisted reproduction technologies outcome of cryopreserved semen from 629 cancer patients.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD1cjntVGmtw%3D%3D&md5=89c5f7362226718c89121a6251e6d6edCAS | 18191846PubMed |
World Health Organization (WHO). (1999). ‘WHO Laboratory Manual for the Examination and Processing of Human Semen.’ 4th edn. (Cambridge University Press: Cambridge, UK.)
World Health Organization (WHO). (2010). ‘WHO Laboratory Manual for the Examination and Processing of Human Semen.’ 5th edn. (WHO Press: Geneva.)
Wyrobek, A. J., Eskenazi, B., Young, S., Arnheim, N., Tiemann-Boege, I., Jabs, E. W., Glaser, R. L., Pearson, F. S., and Evenson, D. (2006). Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm. Proc. Natl Acad. Sci. USA 103, 9601–9606.
| Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XmsVOnsLg%3D&md5=64413e578dfd0eeec5dcc01fd9fc58d6CAS | 16766665PubMed |
Yamauchi, Y., Riel, J. M., and Ward, M. A. (2012). Paternal DNA damage resulting from various sperm treatments persists after fertilization and is similar prior and after DNA replication. J. Androl. 33, 229–238.
| Paternal DNA damage resulting from various sperm treatments persists after fertilization and is similar prior and after DNA replication.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktVyrsb4%3D&md5=e69cfe78ddbf40b855220122fa4f488fCAS | 21546611PubMed |
Zini, A., Boman, J. M., Belzile, E., and Ciampi, A. (2008). Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Hum. Reprod. 23, 2663–2668.
| Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhsVWmt77I&md5=29db695ca6a48596c3c5b4fc29d01b9eCAS | 18757447PubMed |
Zribi, N., Feki Chakroun, N., El Euch, H., Gargouri, J., Bahloul, A., and Ammar Keskes, L. (2010). Effects of cryopreservation on human sperm deoxyribonucleic acid integrity. Fertil. Steril. 93, 159–166.
| Effects of cryopreservation on human sperm deoxyribonucleic acid integrity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXit1Wmt74%3D&md5=ed9418b492991e8fc822ba35ec6a6ea0CAS | 19027111PubMed |
